Response of Bolivian gray titi monkeys (Plecturocebus donacophilus) to an anthropogenic noise gradient: behavioral and hormonal correlates.

Worldwide urban expansion and deforestation have caused a rapid decline of non-human primates in recent decades. Yet, little is known to what extent these animals can tolerate anthropogenic noise arising from roadway traffic and human presence in their habitat. We studied six family groups of titis residing at increasing distances from a busy highway, in a park promoting ecotourism near Santa Cruz de la Sierra, Bolivia. We mapped group movements, sampled the titis' behavior, collected fecal samples from each study group and conducted experiments in which we used a mannequin simulating a human intrusion in their home range. We hypothesized that groups of titi monkeys exposed to higher levels of anthropogenic noise and human presence would react weakly to the mannequin and show higher concentrations of fecal cortisol compared with groups in least perturbed areas. Sound pressure measurements and systematic monitoring of soundscape inside the titis' home ranges confirmed the presence of a noise gradient, best characterized by the root-mean-square (RMS) and median amplitude (M) acoustic indices; importantly, both anthropogenic noise and human presence co-varied. Study groups resided in small, overlapping home ranges and they spent most of their time resting and preferentially used the lower forest stratum for traveling and the higher levels for foraging. Focal sampling analysis revealed that the time spent moving by adult pairs was inversely correlated with noise, the behavioral change occurring within a gradient of minimum sound pressures ranging from 44 dB(A) to 52 dB(A). Validated enzyme-immunoassays of fecal samples however detected surprisingly low cortisol concentrations, unrelated to the changes observed in the RMS and M indices. Finally, titis' response to the mannequin varied according to our expectation, with alarm calling being greater in distant groups relative to highway. Our study thus indicates reduced alarm calling through habituation to human presence and suggests a titis' resilience to anthropogenic noise with little evidence of physiological stress.

Sexual dimorphism in the loud calls of Azara's owl monkeys (Aotus azarae): evidence of sexual selection?

Primates use different types of vocalizations in a variety of contexts. Some of the most studied types have been the long distance or loud calls. These vocalizations have been associated with mate defense, mate attraction, and resource defense, and it is plausible that sexual selection has played an important role in their evolution. Focusing on identified individuals of known sex and age, we evaluated the sexual dimorphism in a type of loud calls (hoots) in a population of wild owl monkeys (Aotus azarae) in Argentina. We found evidence of sexual dimorphism in call structure, with females and males only emitting one type of call, each differing in dominant frequency and Shannon entropy. In addition, both age-related and sex-specific differences in call usage were also apparent in response to the removal of one group member. Future acoustic data will allow us to assess if there are individual characteristics and if the structure of hoot calls presents differences in relation to the social condition of owl monkeys or specific sex responses to variants of hoot calls' traits. This will provide deeper insights into the evolution of vocal mechanisms regulating pair bonding and mate choice strategies in this and other primate species.

Duetting Patterns of Titi Monkeys (Primates, Pitheciidae: Callicebinae) and Relationships with Phylogeny.

Long-range vocal communication in socially monogamous titi monkeys is mediated by the production of loud, advertising calls in the form of solos, duets, and choruses. We conducted a power spectral analysis of duets and choruses (simply "duets" hereafter) followed by linear discriminant analysis using three acoustic parameters-dominant frequency of the combined signal, duet sequence duration, and pant call rate-comparing the coordinated vocalizations recorded from 36 family groups at 18 sites in Bolivia, Peru and Ecuador. Our analysis identified four distinct duetting patterns: (1) a donacophilus pattern, sensu largo, characteristic of P. donacophilus, P. pallescens, P. olallae, and P. modestus; (2) a moloch pattern comprising P. discolor, P. toppini, P. aureipalatii, and P. urubambensis; (3) a torquatus pattern exemplified by the duet of Cheracebus lucifer; and (4) the distinctive duet of P. oenanthe, a putative member of the donacophilus group, which is characterized by a mix of broadband and narrowband syllables, many of which are unique to this species. We also document a sex-related difference in the bellow-pant phrase combination among the three taxa sampled from the moloch lineage. Our data reveal a presumptive taxonomic incoherence illustrated by the distinctive loud calls of both P. urubambensis and P. oenanthe within the donacophilus lineage, sensu largo. The results are discussed in light of recent reassessments of the callicebine phylogeny, based on a suite of genetic studies, and the potential contribution of environmental influences, including habitat acoustics and social learning. A better knowledge of callicebine loud calls may also impact the conservation of critically endangered populations, such as the vocally distinctive Peruvian endemic, the San Martin titi, P. oenanthe.

Song tutoring in presinging zebra finch juveniles biases a small population of higher-order song-selective neurons toward the tutor song.

We explored physiological changes correlated with song tutoring by recording the responses of caudal nidopallium neurons of zebra finches aged P21-P24 (days post hatching) to a broad spectrum of natural and synthetic stimuli. Those birds raised with their fathers tended to show behavioral evidence of song memorization but not of singing; thus auditory responses were not confounded by the birds' own vocalizations. In study 1, 37 of 158 neurons (23%) in 17 of 22 tutored and untutored birds were selective for only 1 of 10 stimuli comprising broadband signals, early juvenile songs and calls, female calls, and adult songs. Approximately 30% of the selective neurons (12/37 neurons in 9 birds) were selective for adult conspecific songs. All these were found in the song system nuclei HVC and paraHVC. Of 122 neurons (17 birds) in tutored birds, all of the conspecific song-selective neurons (8 neurons in 6 birds) were selective for the adult tutor song; none was selective for unfamiliar song. In study 2 with a different sampling strategy, we found that 11 of 12 song-selective neurons in 6 of 7 birds preferred the tutor song; none preferred unfamiliar or familiar conspecific songs. Most of these neurons were found in caudal lateral nidopallium (NCL) below HVC. Thus by the time a bird begins to sing, there are small numbers of tutor song-selective neurons distributed in several forebrain regions. We hypothesize that a small population of higher-order auditory neurons is innately selective for complex features of behaviorally relevant stimuli and these responses are modified by specific perceptual/social experience during development.

In search of the song template.

The auditory template theory-the conversion of memorized song to produced song using feedback as an error-correction mechanism-is central to neurobiological studies of birdsong learning. The essence of the theory is the construction of a complex sound replica based on a set of both genetic and environmental instructions. These premises, as yet unchallenged, have stimulated much research on the process of vocal imitation. Two somewhat distinct, but closely related streams of research have emerged. One seeks to determine the neural mechanisms that underlie the formation, storage, and retrieval of vocal memories as a consequence of experience during a sensitive phase-the template concept in its purest form. The other aims at establishing an explanatory basis for genetically based species differences in auditory responsiveness; here, the prime focus is on innately specified templates that guide learning preferences in young, naïve birds. The chapter begins with an historical overview of conceptual issues. Then recent progress in the attempt to characterize template properties is reviewed, focusing on selected studies of sparrows, nightingales, and zebra finches. The chapter concludes with a discussion of research strategy and tactics, including suggestions for criteria that must be met in identifying neural substrates for template specification and localization. The chapter is intended to provide a conceptual framework for further progress in this critical area.

Metabolic and neural activity in the song system nucleus robustus archistriatalis: effect of age and gender.

The sexually dimorphic robust archistriatal nucleus (RA) represents the telencephalic output of the bird song system. Here, we document sex-dependent changes in both the metabolic and neuronal activity of RA during the sensory and sensorimotor phases of song learning. From posthatching day (PHD) 20-63 in males but not females, RA and its input nucleus HVc showed sharp increases in cytochrome oxidase (CO) activity relative to surrounding archistriatum and the underlying shelf, respectively. In urethane-anesthetized birds, during the same period, the spontaneous activity of male RA neurons underwent dramatic changes in firing rate, distribution of interspike intervals, and bursting frequency, compared with other archistriatal cells. At PHD 20-21, RA neurons had extremely slow, irregular firing rates in birds of both sexes. In males, from PHD 30-36, RA neurons increased their firing rates and spiking activity became more regular, and at approximately PHD 38, strong bursts followed by inhibition (which in awake animals is associated with singing) began to be observed. Dual recordings from RA and HVc revealed synchronous bursting, with RA spikes lagging approximately 10 msec behind HVc. We conclude that changes in relative CO activity correlate with changes in spontaneous firing rates within RA and that patterns of RA spontaneous activity exhibit gradual change as birds enter early song and then again for plastic song. The emergence of strong burst patterns in RA occurs later in life than does input from HVc as established by tracer studies or based on observed HVc bursting in young animals.